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Management of Breast Cancer During Pregnancy Using a Standardized Protocol

From the Departments of Breast Medical Oncology and Surgical Oncology, University of Texas M.D. Anderson Cancer Center; Department of Obstetrics and Gynecology, Baylor College of Medicine; and Department of Obstetrics, Gynecology and Reproductive Sciences, University of Texas Health Science Center, Houston, TX.

Address reprint requests to Richard L. Theriault, DO, Department of Breast Medical Oncology, University of Texas M.D. Anderson Cancer Center, Box 56, 1515 Holcombe Blvd, Houston, TX 77030; email rtheriau{at}mdanderson.org

	ABSTRACT

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PURPOSE: No standardized therapeutic interventions have been reported for patients diagnosed with breast cancer during pregnancy. Of the potential interventions, none have been prospectively evaluated for treatment efficacy in the mother or safety for the fetus. We present our experience with the use of combination chemotherapy for breast cancer during pregnancy.

PATIENTS AND METHODS: During the past 8 years, 24 pregnant patients with primary or recurrent cancer of the breast were managed by outpatient chemotherapy, surgery, or surgery plus radiation therapy, as clinically indicated. The chemotherapy included fluorouracil (1,000 mg/m²), doxorubicin (50 mg/m²), and cyclophosphamide (500 mg/m²), administered every 3 to 4 weeks after the first trimester of pregnancy. Care was provided by medical oncologists, breast surgeons, and perinatal obstetricians.

RESULTS: Modified radical mastectomy was performed in 18 of the 22 patients, and two patients were treated with segmental mastectomy with postpartum radiation therapy. This group included patients in all trimesters of pregnancy. The patients received a median of four cycles of combination chemotherapy during pregnancy. No antepartum complications temporally attributable to systemic therapy were noted. The mean gestational age at delivery was 38 weeks. Apgar scores, birthweights, and immediate postpartum health were reported to be normal for all of the children.

CONCLUSION: Breast cancer can be treated with chemotherapy during the second and third trimesters of pregnancy with minimal complications of labor and delivery.

	INTRODUCTION

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BREAST CANCER diagnosed during pregnancy can be devastating for the patient and her family. Active treatment of the malignancy and continuation of the pregnancy are often presented as mutually exclusive options, pitting the life of the mother against that of her unborn child. Because of the hormonally responsive nature of the breast and the exponential increases in estrogens and progestins seen during pregnancy, abortion is often recommended to avoid possible potentiation of tumor growth and to permit traditional treatments. However, patient survival has not been reported to be improved by pregnancy termination.^1-4

Breast cancer is the most common malignancy associated with pregnancy, with an increasing prevalence with increasing maternal age (Fig 1).⁵ With trends toward delayed childbearing, breast malignancies diagnosed during pregnancy are expected to become more common.⁶ Although the frequency of the coincidental diagnosis averages 1 in 3,000 pregnancies, few obstetricians, surgeons, or oncologists have experience in caring for the pregnant patient with breast cancer.⁶

View larger version (28K): [in this window] [in a new window]   Fig 1. Age-specific prevalence of malignancies in women of childbearing age, 1984 to 1988. Adapted.5

Breast cancer is optimally treated with multimodality therapy, which may include surgical resection, radiation therapy, and systemic chemotherapy. A similar treatment strategy can be used for breast cancer during pregnancy. Although radiation therapy is contraindicated during pregnancy, chemotherapy has been used successfully without apparent harm to the mother or fetus.^6-8 Certain chemotherapeutic agents have been shown to be teratogenic during the first trimester. However, Weibe and Sipila,⁷ in their review of the use of chemotherapeutic drugs during pregnancy, substantiated the relative safety of the majority of chemotherapy agents when administered during the second and third trimesters.

Despite the availability of retrospective case reports and case series, no standardized prospective experience is available for evaluation of the maternal response to and adverse fetal effects of medical therapies for breast cancer during pregnancy. We present an 8-year experience of an ongoing, standardized, multidisciplinary treatment program for the management of breast cancer during pregnancy.

	PATIENTS AND METHODS

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Before 1992, the treatment recommendations for the pregnant patient with breast cancer were made by a consensus decision of breast surgeons and radiation and medical oncologists. In 1992, the treatment approach was formalized in a clinical practice protocol that was approved by the institutional review board (IRB) of the University of Texas M.D. Anderson Cancer Center. All subjects participating in this trial provided written informed consent, and all results are presented with the approval of the IRB. The informed consent (Appendix) was developed by the members of the Department of Breast Medical Oncology. It has not been modified except for administrative requirements of the IRB and/or the United States Office for Protection From Research Risks.

Treatment Protocol
Initially, each patient provided a complete history and underwent a physical examination by a medical or surgical oncologist. The breast mass was imaged by ultrasonography, mammography with abdominal shielding, or both. Fine-needle aspiration or core-needle biopsy under local anesthesia was performed for clinically palpable masses. An excisional biopsy, also under local anesthesia, was performed for nonpalpable masses or palpable masses with a nondiagnostic needle biopsy. The metastatic work-up included a two-view chest x-ray with abdominal shielding, a complete blood cell count, and renal and liver function tests.

Once a diagnosis of invasive malignancy was established, the patient was referred to a specialist of maternal-fetal medicine for an accurate assessment of gestational age by ultrasonography. Genetic counseling was offered, with an emphasis on the potential effects of chemotherapy on the fetus. The patient was given the option of terminating the pregnancy or continuing it with or without active cancer treatment. Information was provided about the known potential risks and benefits of each option.

Surgical consultation was requested for patients who opted to continue the pregnancy and for treatment of those who had operable disease at presentation. For the majority of surgically resectable tumors, modified radical mastectomy with axillary lymph node dissection was performed, regardless of gestational age. At the time of surgery, tissue samples were submitted for pathologic staging, histologic examination, nuclear grading, and determination of hormone receptor status. All tissue specimens from patients with surgical resections performed at other institutions were reviewed by the Department of Pathology at M.D. Anderson Cancer Center. Stage IV or recurrent tumors were confirmed by biopsy, if clinically warranted, and treated with chemotherapy without major surgical procedures. Patients with stage III tumors received neoadjuvant chemotherapy (up to four cycles) before receiving locoregional therapy.

Each patient had a central venous catheter placed for long-term venous access. Outpatient combination chemotherapy with cyclophosphamide (500 mg/m² intravenously in a single dose on day 1), doxorubicin (50 mg/m² by continuous intravenous infusion over 72 hours), and two bolus doses of fluorouracil (500 mg/m² intravenously on days 1 and 4) (FAC) was administered every 21 to 28 days during the second and third trimesters of pregnancy through week 37. The patients were monitored with complete blood cell counts and liver and renal function tests, as clinically warranted. Nausea and vomiting were treated with intravenous or oral ondansetron hydrochloride (Zofran; Glaxo Pharmaceuticals, Research Triangle Park, NC) or with promethazine or prochlorperazine tablets or suppositories. Interruption of or delays in chemotherapy administration occurred only for drug-related toxicity or patient refusal to continue.

High-risk obstetric care was provided with an emphasis on intensive fetal surveillance. Serial fetal growth ultrasound examinations were performed every 3 to 4 weeks or as clinically warranted. Fetal nonstress testing or biophysical profiles were performed between 28 weeks' gestation and term. Amniocenteses were offered for standard obstetric indications. Likewise, preterm deliveries were performed only for obstetric indications. Idiopathic preterm labor was actively treated with parenteral tocolytics and corticosteroids until 34 weeks' gestation to lessen the neonatal sequelae of prematurity.

Clinical Assessments and Statistical Analysis
Outcomes were assessed by determination of antepartum complications, gestational age at delivery, labor and delivery complications, birthweight, Apgar scores, and postpartum complications. Maternal survival and disease-free intervals are reported. Data are reported as statistical means ± standard deviations for normally distributed continuous variables and as medians (ranges) for nonparametric data.

	RESULTS

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Since April 1989, 26 pregnant patients with a concurrent diagnosis of a primary or recurrent breast malignancy have been treated. Two patients were excluded from evaluation. One patient had previously received chemotherapeutic agents during the reference pregnancy, and one was treated and observed at an out-of-state institution, and medical records could not be obtained. Therefore, 24 patients are included in our analysis. The demographics of our population are presented in Table 1. Nineteen (79%) of the women in the study were white, three (13%) were Hispanic, one (4%) was African-American, and one (4%) was Arabic.

Twenty-two patients were diagnosed with primary breast cancers intact. Two patients with previous histories of primary breast lesions were diagnosed with recurrent disease. Modified radical mastectomies were performed without complications in 18 of the 22 patients with primary cancers, in 14 patients during pregnancy and in four patients postpartum after chemotherapy for locally advanced breast cancer. First-trimester surgery was performed in four (29%) of 14 patients with no subsequent spontaneous abortions. Second- or third-trimester surgery was performed in the remaining 10 patients (71%), also with no fetal compromise or preterm labor. Two patients had antepartum segmental mastectomy with axillary lymph node dissection followed by chemotherapy and postpartum radiation therapy. Three patients with stage IV disease did not have surgery as part of the treatment plan, and one patient refused surgery and/or locoregional radiation therapy postpartum.

The stage and histologic type of the primary tumors are listed in Table 2. The median primary tumor size was 4.5 cm (range, 1.4 to 7 cm). Sixty-seven percent of the tumors were lymph node positive at the time of surgery. Poorly differentiated tumors comprised 76% of the primary cancers. Twenty-four percent were moderately differentiated. None of the primary cancers was well differentiated. Fifteen percent of the primary tumors were positive for both estrogen and progesterone receptors, 10% were positive for estrogen receptors but not progesterone receptors, 10% were positive for progesterone receptors but not estrogen receptors, and 65% were negative for both receptors.

The patients tolerated full doses of chemotherapy without major complications. Granulocytopenia occurring at the nadir required no intervention in any of the patients. The number of chemotherapy cycles and the cumulative doses of each drug received during pregnancy are listed in Table 3.

There were no unexpected antepartum maternal complications. One patient was hospitalized for diarrhea and suspected (but unconfirmed) pyelonephritis, both of which resolved with symptomatic and supportive care. One patient required hospital admission for intravenous administration of heparin because of deep venous thrombosis of the calf. The patient had previously experienced a deep venous thrombosis in the same lower extremity. Preterm labor occurred in three patients (12%), and severe pre-eclampsia was noted in one (4%). None of these complications was temporally related to the medical or surgical treatment for the malignancy.

The median gestational age at delivery was 38 weeks (range, 33 to 40 weeks). Three patients delivered before term, one as a consequence of pre-eclampsia, and two because of idiopathic preterm labor (8%). Two cases of postpartum endometritis (8%) resolved with administration of intravenous antibiotics. Lactation in the postpartum period was impaired, and breast-feeding was proscribed as a consequence of chemotherapy exposure.

The neonates experienced no unusual complications. The Apgar scores at birth were uniformly 9 or greater at 5 minutes of life. None of the 24 infants was congenitally malformed. The birthweights are graphed by gestational age in Fig 2.⁹ Only one infant had a birthweight lower than the 10th percentile for gestational age. One infant was diagnosed with hyaline membrane disease secondary to prematurity. This infant, who was delivered at 33 weeks owing to pre-eclampsia, recovered with no complications. Two infants required brief periods of oxygen support for transient tachypnea of the newborn; in both, tachypnea resolved within 48 hours. The only complication readily attributable to chemotherapy occurred after the preterm delivery of an infant 2 days after the last chemotherapy dose. This infant developed transient leukopenia without infectious sequelae. The neonatal nadir occurred concurrently with the maternal WBC count nadir, and neither mother nor child required medical intervention. Despite maternal alopecia, only two of the neonates were reported to have substantial hair loss.

View larger version (15K): [in this window] [in a new window]   Fig 2. Gestational age and birthweight comparison of infants exposed to chemotherapeutic drugs in utero. Adapted with permission.9

At the time of this report, the median age of the children is 4.5 years (range, 6 months to 8 years). Maternal survival data are presented in Table 4. The three patients with recurrent tumors or stage IV tumors at presentation died of disease within 2 years of diagnosis. The stage I patient was diagnosed with recurrence at 37 months. Six (67%) of the nine stage II patients are alive at a median of 44 months of follow-up (range, 9 to 88 months), and all are disease free. At a median follow-up of 36 months (range, 14 to 73 months), nine (82%) of 11 stage III patients are alive, and eight of 11 (72%) are alive without disease. At a median of 40 months, the combined survival rate for women with stage II or III disease is 75%, and the disease-free survival rate is 70%.

	DISCUSSION

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The frequency of breast cancer coincidental with pregnancy is estimated to be between 1 in 1,360 and 1 in 3,200.^10-12 White¹¹ reported that 2.8% of 45,881 women with cancer of the breast had a concurrent or recent pregnancy. Similarly, it has been reported that up to 7.3% of women younger than 45 years of age with a breast malignancy are pregnant or lactating.¹³

Delays in diagnosing breast masses during pregnancy are common. The hypertrophy and engorgement of the breasts in response to the hormonal changes of pregnancy may make both physical examination and mammographic imaging more difficult than in the nonpregnant patient. Many masses discovered during pregnancy and lactation are attributed to physiologic changes and may be discounted by the patient.⁶ Because of patient and physician reluctance to pursue definitive diagnostic procedures such as biopsy for breast masses during pregnancy, the average time from the onset of symptoms to diagnosis is much longer in pregnant than in nonpregnant women: 11 months versus 4 months.¹³ The indications for mammography, fine-needle aspiration, core biopsy, and open breast biopsy are identical in the pregnant and nonpregnant patient.

The prognosis for breast cancer is generally thought to be worsened by the coexistence of pregnancy. Despite the responsiveness of breast tissue to the hormonal stimulation of pregnancy and lactation, when controlled for patient age and disease stage, survival of the pregnant and nonpregnant breast cancer patient has been reported to be equal.^4,14,15 Similarly, the prognosis does not appear to be improved for the pregnant patient who aborts the pregnancy and receives standard treatment for the disease.¹⁶ Even in advanced stages, elective abortion in combination with castration (bilateral oophorectomy) to decrease the potential hormonal stimulation of breast cancers has not been shown to improve survival.^17,18 Termination of pregnancy is not an effective therapeutic intervention.

Since radiation is a cause of congenital birth defects, the diagnostic and staging evaluations for the pregnant breast cancer patient can be modified to limit fetal exposure.¹⁹ We have used shielded chest x-rays, which limit total fetal radiation exposure to 0.00008 Gy, substantially less than the accepted level of fetal exposure of 0.05 Gy.²⁰ Ultrasonography is the preferred imaging modality because of the radiodensity of the breast in the pregnant or lactating woman. This technique eliminates the radiation exposure of mammography. However, mammography with proper shielding creates little potential for fetal exposure. The search for distant metastases to the abdomen and pelvis may be safely performed with ultrasonography or magnetic resonance imaging.²¹ Bone scans, although rarely used, result in only 0.00194 Gy of radiation exposure to the fetus.⁶ Although external-beam radiation therapy may be used in the primary treatment of the nonpregnant patient, the scatter from such therapy would be prohibitive during gestation and therefore was not included in our treatment plan.

Major surgical procedures are not routinely performed during pregnancy. However, they are not uncommon. Haagensen and Stout²² concluded that mastectomy should be avoided during pregnancy and lactation. This position was subsequently retracted.²³ Since then, many authors have reiterated that mastectomy can be performed safely throughout pregnancy without significant risks of fetal injury or spontaneous abortion.^{1,11,18,19,24} Likewise, general anesthesia for mastectomy during pregnancy presents no substantially increased risk to the mother or the fetus.²⁵

Conflicting opinions exist regarding the safety and possible adverse fetal effects of the use of chemotherapy during pregnancy. Weibe and Sipila⁷ reviewed the literature regarding each of the commonly used chemotherapeutic agents and their effect on gestation. Unfortunately, retrospective reviews and case reports form the basis for conclusions on this topic. Many reports involve exposure to multiple chemotherapy agents as well as radiation during various times throughout pregnancy. The highest risk of congenital malformations occurs when a first-trimester fetus is exposed to multiple cytotoxic agents in combination with radiation. No cases of malformed fetuses in the absence of first-trimester chemotherapy and radiation were noted. The chemotherapeutic agents (FAC) and dosing regimen administered in the current study are used in the standard chemotherapy protocols for the nonpregnant patient with invasive breast carcinoma. The only modification is the general avoidance of first-trimester exposure. Only one patient in this series was treated during the first trimester (at 11 weeks). All of the agents used are considered pregnancy category D (teratogenic potential demonstrated in animals). However, none of these agents has been evaluated prospectively in human trials. The FAC protocol reported here has not resulted in any detectable congenital anomalies when administered after the first trimester. Similarly, the incidences of preterm labor and pre-eclampsia observed were equal to those of the published background population, suggesting no adverse obstetric side effects.^26,27

In 1968, Nicholson²⁸ reported a 40% incidence of low birthweight among infants born to mothers exposed to chemotherapy in utero. Contrary to these findings, we found no increase in low birthweight in infants born to the mothers exposed to FAC.

As with breast cancer in the general population, the majority of patients in our study had primary ductal adenocarcinomas. Most of these tumors were poorly differentiated and were negative for both estrogen and progesterone receptors, a finding similar to those of previous reports.³ The incidence of inflammatory cancer (4.2%) is similar to the incidence noted in the literature (1.5% to 4%).^29-31 The high percentage of poorly differentiated tumors and the high percentage of node-positive tumors may be responsible for the previously reported poor prognosis for breast cancer diagnosed during pregnancy. The incidence of node-positive tumors in our series was similar to that reported in previously published series^13,17,30 and may reflect the delays in breast cancer diagnosis associated with pregnancy.

Survival for patients with breast cancers during pregnancy is generally considered poor. However, many authors have reported similar survival, stage for stage, of the pregnant and nonpregnant woman.^3,13,15 The survival of our patients has been promising. However, to date, only eight patients with stage II or III disease have been followed to the fifth year. Further follow-up and a larger number of patients will be necessary to validate survival data.

This study represents the first standardized, prospective evidence that primary and recurrent breast cancer can be treated during pregnancy without demonstrable harm to the fetus. Despite the perceived risk to the fetus from chemotherapy exposure, no congenital malformations or immediate postpartum deficits have been apparent after exposure to FAC administered to pregnant women during the second and third trimesters. A comprehensive, multidisciplinary approach to the management of these patients allows for the continuation of pregnancy. When this approach is used, the breast malignancy may be treated effectively without sacrificing the life of the fetus or compromising the health of the mother.

[View Appendix]

View larger version (257K): [in this window] [in a new window]   APPENDIX

	NOTES

 
Presented in part at the Annual Meeting of the American Society of Clinical Oncology, San Diego, CA, May 20-23, 1992; the 9th International Congress on Breast Disease, Houston, TX, April 28-May 2, 1996; and Biomedicine `96: Medical Research from Bench to Bedside, Washington, DC, May 3-6, 1996.

	REFERENCES

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1. Hubay CA, Barry FM, Marr CC: Pregnancy and breast cancer. Surg Clin North Am 58:819-831, 1978[Medline]

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3. Nugent P, O'Connell TX: Breast cancer and pregnancy. Arch Surg 120:1221-1224, 1985[Abstract/Free Full Text]

4. Barnovan Y, Wallack MK: Management of the pregnant patient with carcinoma of the breast. Surg Gynecol Obstet 171:347-352, 1990[Medline]

5. Ries LAG, Hankey BF, Miller BA, et al (eds): Cancer Statistics Review 1973-1988. Bethesda, MD, National Cancer Institute, NIH publication 91-2789, III.39, 1991

6. Donegan WL: Breast carcinoma and pregnancy, in Donegan WL, Spratt JS (eds): Cancer of the Breast (ed 4). Philadelphia, PA, Saunders, 1995, pp 732-741

7. Weibe VJ, Sipila PEH: Pharmacology of antineoplastic agents in pregnancy. Crit Rev Oncol Hematol 16:75-112, 1994[Medline]

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9. Lubchenco LO, Hansman C, Boyd E: Intrauterine growth in length and head circumference as estimated from live births at gestational ages from 26 to 42 weeks. Pediatrics 37:403-408, 1966[Abstract/Free Full Text]

10. Finn WF: Pregnancy complicated by cancer. Bull Margaret Hague Maternity Hosp 5:2-6, 1952

11. White TT: Prognosis for breast cancer for pregnant and nursing women: Analysis of 1413 cases. Surg Gynecol Obstet 100:661-666, 1955[Medline]

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14. Rissanen PM: Carcinoma of the breast during pregnancy and lactation. Br J Cancer 22:663-668, 1968[Medline]

15. Peters MV: The effect of pregnancy in breast cancer, in Forrest APM, Kunkler PB, (eds): Prognostic Factors in Breast Cancer. Edinburgh, United Kingdom, Livingstone, 1968, pp 65-89

16. Bush H, McCredie JA: Carcinoma of the breast during pregnancy and lactation, in Allen HH, Nisker JA (eds): Cancer in Pregnancy: Therapeutic Guidelines. Mount Kisco, NY, Futura, 1986, pp 91-101

17. Holleb AI, Farrow JH: The relation of carcinoma of the breast and pregnancy in 283 patients. Surg Gynecol Obstet 115:65-71, 1962[Medline]

18. Bunker ML, Peters MV: Breast cancer associated with pregnancy or lactation. Am J Obstet Gynecol 85:312-321, 1963

19. Theriault RL, Hortobagyi GN: When breast cancer complicates pregnancy: What options are available? Prim Care Cancer 9:27-32, 1989

20. Brent RL: Ionizing radiation. Contemp Ob/Gyn 30:20-29, 1987

21. Cunningham FG, McDonald PC, Gant NF, et al: Neoplastic diseases, in Williams Obstetrics (ed 19). Norwalk, CT, Appleton and Lange, 1993, pp 1267-1270

22. Haagensen CD, Stout AP: Carcinoma of the breast: Criteria of operability. Ann Surg 118:859-870, 1943[Medline]

23. Haagensen CD: Diseases of the Breast (ed 1). Philadelphia, PA, Saunders, 1956, p 538

24. Kilgore AR, Bloodgood JC: Tumors and tumor-like lesions of the breast in association with pregnancy and lactation. Arch Surg 18:2079-2098, 1929[Abstract/Free Full Text]

25. Mazze RI, Kallen B: Reproductive outcome after anesthesia and operation during pregnancy: A registry study of 5405 cases. Am J Obstet Gynecol 161:1178-1185, 1989[Medline]

26. Creasy RK: Preterm labor and delivery, in Creasy RK, Resnik R (eds): Maternal-Fetal Medicine: Principles and Practice (ed 3). Philadelphia, PA, Saunders, 1994, p 494

27. American College of Obstetricians and Gynecologists: Hypertension in Pregnancy. ACOG Technical Bulletin 219. Washington, DC: American College of Obstetricians and Gynecologists, 1996

28. Nicholson HO: Cytotoxic drugs in pregnancy. J Obstet Gynecol Br Commonw 75:307-312, 1968[Medline]

29. Clark RM, Reid J: Carcinoma of the breast in pregnancy and lactation. Int J Radiat Oncol Biol Phys 4:693-698, 1978[Medline]

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31. Rosemond GP: Management of patients with carcinoma of the breast in pregnancy. Ann NY Acad Sci 114:851-860, 1964[Medline]

Submitted June 4, 1998; accepted November 5, 1998.

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